Male-limited secondary sexual trait interacts with environment in determining female fitness

Abstract

Selection for secondary sexual trait (SST) elaboration may increase intralocus sexual conflict over the optimal values of traits expressed from shared genomes. This conflict can reduce female fitness, and the resulting gender load can be exacerbated by environmental stress, with consequences for a population's ability to adapt to novel environments. However, how the evolution of SSTs interacts with environment in determining female fitness is not well understood. Here, we investigated this question using replicate lines of bulb mites selected for increased or decreased prevalence of a male SST—thickened legs used as weapons. The fitness of females from these lines was measured at a temperature to which the mites were adapted (24°C), as well as at two novel temperatures: 18°C and 28°C. We found the prevalence of the SST interacted with temperature in determining female fecundity. At 28°C, females from populations with high SST prevalence were less fecund than females from populations in which the SST was rare, but the reverse was true at 18°C. Thus, a novel environment does not universally depress female fitness more in populations with a high degree of sexually selected dimorphism. We discuss possible consequences of the interaction we detected for adaptation to novel environments.

Sexual selection, environmental robustness, and evolutionary demography of maladapted populations: A test using experimental evolution in seed beetles

“…These costs and benefits of sexual selection may produce variable outcomes at the population level, as observed in experimental systems providing evidence for sexual selection increasing adaptation (Fricke & Arnqvist, ; Grieshop, Stångberg, Martinossi‐Allibert, Arnqvist, & Berger, ; Mallet, Bouchard, Kimber, & Chippindale, ; Mcguigan, Petfield, & Blows, ; Plesnar‐Bielak, Skrzynecka, Prokop, & Radwan, ; Sharp & Agrawal, ) as well as impeding it (Arbuthnott & Rundle, ; Berger, Martinossi‐Allibert et al, ; Chenoweth, Appleton, Allen, & Rundle, ; Holland, ; Hollis & Houle, ; Rundle, Chenoweth, & Blows, ). The impact of environmental change on these dynamics has started to be explored in recent years (Arbuthnott, Dutton, Agrawal, & Rundle, ; Berger et al, ; Connallon & Clark, ; Gerber & Kokko, ; Gomez‐Llano, Bensch, & Svensson, ; Holman & Jacomb, ; Li & Holman, ; Martinossi‐Allibert, Rueffler et al, ; Martinossi‐Allibert, Savković et al, ; Parrett & Knell, ; Plesnar‐Bielak et al, ; Punzalan, Delcourt, & Rundle, ; Skwierzyńska, Radwan, & Plesnar‐Bielak, ; Yun et al, ), and there are indeed reasons to suspect that the different facets of sexual selection will be sensitive to rapid ecological change. For example, male reproductive traits often exhibit genotype‐by‐environment interactions (GEI:s) (Bussiere, Hunt, Stölting, & Jennions, ; Kolluru, ; Miller & Svensson, ).…”

Sexual conflict in a changing environment

“…Most studies measured intersexual genetic correlations for fitness (r MF ) in two or more environments, but other designs have also been incorporated (see online Supporting information, Table S1 ). Some studies supported the idea that IASC is most pronounced in environments to which a population is adapted and declines in a novel environment and/or under stress (Long et al ., 2012 ; Punzalan et al ., 2014 ; Han & Dingemanse, 2017 ), while others found similar levels of IASC across environments or even increased conflict in stressful environments (Delcourt et al ., 2009 ; Delph et al ., 2011 a ; Martinossi‐Allibert, Arnqvist & Berger, 2017 ; Koch et al ., 2020 ; see also Skwierzyńska, Radwan & Plesnar‐Bielak, 2018 ). The reason for these discrepancies is intriguing, given that they can be found even when the same species and environmental modifications are used [compare Delcourt et al .…”

“…Similarly, Skwierzyńska et al . ( 2018 ) demonstrated costs for females carrying genes associated with the expression of a male‐limited sexually selected trait (thickened legs used as a weapon and the associated aggressive strategy of ‘fighter’ male phenotype; see Appendix S1) in the bulb mite Rhizoglyphus robini at high, stressful temperature, but not at low temperature. This low temperature, while novel to the animals tested, is probably associated with milder stress.…”

“…While such an approach allows careful control of experimental conditions of interest, the complexity of natural environments, with spatial and temporal variation of many interacting environmental variables, may generate IASC patterns that differ from those observed in laboratories. For example, laboratory studies have tested pure effects of temperature on IASC (Berger et al ., 2014 ; Skwierzyńska et al ., 2018 ), but variance in temperature is usually correlated with other climatic factors like relative humidity, water availability etc., that together may influence IASC. In addition, these climatic factors often vary temporally, in contrast to stable laboratory conditions.…”

“…Both IASC and IESC might be affected by environmental conditions, and this effect might be more pronounced in relation to one or the other type of conflict. For example, it seems that decreased temperature removes IASC over the expression of genes associated with male morphs in the bulb mite (Plesnar‐Bielak et al ., 2018 ; Skwierzyńska et al ., 2018 ). At the same time, it reduces the selective advantage of the 6Pdgh allele associated with increased male competitiveness and lowered fitness of females mating with males possessing this allele (Plesnar‐Bielak, Skwierzyńska & Radwan, 2020 ; see Appendix S1), thus also relaxing IECS.…”